ORIGINAL RESEARCH published: 18 June 2021 doi: 10.3389/fnhum.2021.617596
Dose-Response Effects of Acute Aerobic Exercise Intensity on Inhibitory Control in Children With Attention Deficit/Hyperactivity Disorder
Yu-Jung Tsai 1, Shu-Shih Hsieh 2, Chung-Ju Huang 3 and Tsung-Min Hung 1,4*
1 Department of Physical Education and Sport Sciences, National Taiwan Normal University, Taipei, Taiwan, 2 Department of Psychology, Northeastern University, Boston, MA, United States, 3 Graduate Institute of Sport Pedagogy, University of Taipei, Taipei, Taiwan, 4 Institute for Research Excellence in Learning Science, National Taiwan Normal University, Taipei, Taiwan
The present study aimed to examine whether the effect of acute aerobic exercise on inhibitory control of children with attention-deficit/hyperactivity disorder (ADHD) is moderated by exercise intensity. Using a within-subjects design, 25 children with ADHD completed a flanker task with concurrent collection of electroencephalography (EEG) data after three different intensities of treadmill running. The results showed that
Edited by: low- and moderate-intensity exercises resulted in shorter reaction times (RTs) relative Sebastian Ludyga, to vigorous-intensity exercise during the incompatible condition of the flanker task University of Basel, Switzerland regardless of task congruency. A P3 congruency effect was observed following low- and Reviewed by: vigorous-intensity exercises but not after moderate-intensity exercise. The mean alpha Aylin Mehren, University of Oldenburg, Germany power, a measure of cortical arousal, increased following low- and moderate-intensity Manuel Mücke, exercises but decreased following vigorous-intensity exercise. In addition, the change in University of Basel, Switzerland arousal level after moderate-intensity exercise was negatively correlated with RT during *Correspondence: Tsung-Min Hung incompatible flanker tasks. The current findings suggest that children with ADHD have [email protected] better inhibitory control following both low- and moderate-intensity exercises relative to vigorous aerobic exercise, which could be characterized by an optimal state of Specialty section: cortical arousal. This article was submitted to Brain Health and Clinical Keywords: intensity, acute exercise, executive function, arousal level, ADHD Neuroscience, a section of the journal Frontiers in Human Neuroscience INTRODUCTION Received: 04 November 2020 Accepted: 17 May 2021 A deficit in executive function is one of the core cognitive deficits in attention-deficit/hyperactivity Published: 18 June 2021 disorder (ADHD) (Willcutt et al., 2005), a condition which can persist from early childhood to Citation: young adulthood (Biederman et al., 2011; Lin and Gau, 2018). In particular, deficits in inhibitory Tsai Y-J, Hsieh S-S, Huang C-J and control in children with ADHD have been considered as an endophenotype (McAuley et al., Hung T-M (2021) Dose-Response 2014). Inhibitory control refers to withholding the attention of an individual in response to task- Effects of Acute Aerobic Exercise irrelevant but prepotent information and stays focused on goal-relevant information (Barkley, Intensity on Inhibitory Control in Children With Attention 1997). Children with ADHD have demonstrated weaker inhibitory control signified by longer Deficit/Hyperactivity Disorder. reaction times (RTs) and lower levels of accuracy during neuropsychological testing, compared with Front. Hum. Neurosci. 15:617596. typically developing children (Mullane et al., 2009). Impaired inhibitory control has been associated doi: 10.3389/fnhum.2021.617596 with failures in several cognitive processes such as attention allocation, stimuli evaluation, as well as
Frontiers in Human Neuroscience | www.frontiersin.org 1 June 2021 | Volume 15 | Article 617596 Tsai et al. Exercise Intensity and Inhibitory Control action monitoring (Doehnert et al., 2010; Liotti et al., 2010; there may be a dose-response effect of acute aerobic exercise Kratz et al., 2011). Given that inhibitory control is one intensity on inhibitory control in children with ADHD. of the cornerstones of complex cognitive operations (e.g., The differential effects of low, moderate, and vigorous- cognitive flexibility and planning) (Miyake et al., 2000), and intensity aerobic exercises on inhibitory control may be that deficits in this cognitive domain are one of the neuro- accounted for, at least in part, by fluctuations in cortical arousal. pathologies in children with ADHD (McAuley et al., 2014), Davey (1973) postulates that moderate-intensity aerobic exercise understanding approaches that facilitate inhibitory control may results in an optimal level of cortical arousal, which, in turn, be of significance. facilitates cognitive performance, whereas low- and vigorous- A growing body of evidence has demonstrated a positive intensity exercise may lead to suboptimal and excessive cortical effect of acute aerobic exercise on inhibitory control in children arousal, thereby compromising cognitive performance. This with ADHD (Chang et al., 2012; Pontifex et al., 2013; Chuang inverted-U shape relation has been verified in non-clinical, et al., 2015; Piepmeier et al., 2015). In particular, previous studies typically developed populations (Kamijo et al., 2004a; Chang suggested that moderate-intensity aerobic exercise, defined either and Etnier, 2009; Chang et al., 2011), but remain underexplored as 50–70% of heart rate reserve (HRR) (Chang et al., 2012; in children with ADHD. Hypoarousal has been consistently Chuang et al., 2015; Yu et al., 2020) or 60–75% of maximal reported in children with ADHD (Satterfield et al., 1974; HRR (Pontifex et al., 2013; Piepmeier et al., 2015), facilitates Barry et al., 2003; Rowe et al., 2005). The optimal stimulation inhibitory control in children with ADHD. However, the effect of (OS) model suggested that the state of arousal of the central low (<40% HRR) and vigorous-intensity (>70% HRR) exercises nervous system (CNS) drives subsequent response and behavior on inhibitory control in children with ADHD is still unclear. (Zentall and Zentall, 1983). According to the OS model, Two studies reported that vigorous-intensity aerobic exercise hypoarousal in children with ADHD, probably results from benefits inhibitory control in children with ADHD. Specifically, deviated maturation/dysfunction in the prefrontal cortex (Strauß Gawrilow et al. (2016) found that children with ADHD exhibited et al., 2018; Zhang et al., 2018), is closely related to inattention better inhibitory control following a single bout of vigorous- and hyperactivity (Rapport et al., 2009). Given the modulatory intensity aerobic exercise. Similarly, Silva et al. (2015) found that effect of acute exercise on arousal (Kamijo et al., 2004a; Chang children with ADHD who underwent vigorous-intensity exercise et al., 2011), it is reasonable to postulate that better cognitive workouts demonstrated identical levels of attention as their performance following acute exercise may be mediated by an typically developing peers, who received no exercise intervention. upregulation of cortical arousal. However, findings from these two studies are confounded by To measure cortical arousal, the current study used alpha the use of between-subjects design with no pre-test measures, oscillations from electroencephalography (EEG). Alpha power, in which pre-existing differences between intervention groups or the amplitude of brainwaves between 8 and 13 Hz frequency cannot be assessed. In addition, one study investigating the band, has been shown to be inversely correlated with mental effects of high-intensity interval exercise found a positive effect activity. Studies also show a relationship between reduced alpha on sustained attention, but findings are confounded by unequal power (i.e., EEG desynchrony) and increased vigilance, alertness, durations between the exercise and non-active control condition and attention (see Oken et al., 2006 for a comprehensive (Medina et al., 2010). Another study employing the same exercise review). Furthermore, attenuation of alpha oscillation is inversely mode and cognitive task found no effect of high-intensity interval associated with fMRI blood-oxygen-level dependent (BOLD) exercise on sustained attention, but in this case, the results are cortical response (Laufs et al., 2006) and is closely related to confounded by individual differences in medication use (Mahon another standardized measure of arousal, skin conductance, with et al., 2013). reduced alpha activity relates to increased skin conductance Moreover, although no previous study investigated the (Barry et al., 2005). These data suggest that reduction in alpha differential effects across low, moderate, and vigorous-intensity power is associated with increased cortical arousal, but despite aerobic exercises on inhibitory control in children with ADHD, this relation, alpha oscillation has not been broadly utilized a meta-analysis of individuals without ADHD indicated that in studying the relationship between exercise, arousal, and high- and moderate-intensity exercises, but not light-intensity cognition in children with ADHD. exercise, benefits cognitive function in adults over 50 years old The Ericksen flanker task has been extensively used to (Northey et al., 2018). In contrast, another meta-analysis found measure inhibitory control in children with ADHD (Mullane that the beneficial effect of vigorous-intensity exercise and high- et al., 2009). It involves participants being instructed to identify a intensity interval training were larger than moderate-intensity target stimulus defined by its directionality (i.e., the directionality exercise (Oberste et al., 2019). In addition, a systematic review of an arrow) while ignoring other distracting stimuli that found a beneficial effect of low-intensity exercise on cognitive flanking the target stimulus. In general, children with ADHD performance (i.e., word fluency) in older adults (Tse et al., 2015). display longer RT (Liu et al., 2020) and lower response An empirical study further indicated that young adults had accuracy (Johnstone and Galletta, 2013) compared with typically better inhibitory control performance following a single bout developing children during the flanker task. of low-intensity aerobic exercise relative to following a control In addition to behavioral indices, event-related brain condition (Byun et al., 2014). These findings, altogether, suggest potentials (ERPs) from EEG affords insights into the specific that exercise intensity is an important factor when assessing cognitive processes underpinning inhibitory control (Luck, cognitive performance in individuals without ADHD and that 2014). In particular, the amplitude and latency of the P3-ERP
Frontiers in Human Neuroscience | www.frontiersin.org 2 June 2021 | Volume 15 | Article 617596 Tsai et al. Exercise Intensity and Inhibitory Control have been demonstrated to represent the allocation of attention diagnosed with ADHD by a certified psychiatrist by following resources and speed of stimulus processing/evaluation, the diagnosis criteria by the DSM-IV (Diagnostic and Statistical respectively (Polich, 2007). Pontifex et al. (2013) reported Manual of Mental Disorders, Fourth Edition); (2) aged between7 that, during a flanker task, children with ADHD displayed larger and 12 years; and (3) no history of brain injury or neurological P3 amplitudes following a 20 min bout of moderate-intensity conditions, such as epileptic seizures, serious head injuries, or aerobic exercise relative to the following reading. Similarly, periods of unconsciousness. Ludyga et al. (2017) found that in children with ADHD, there For supplementary assessments to further verify symptoms were increased P3 amplitudes during a flanker task following of ADHD, the Chinese version of the ADHD test originally a single bout of 20 min moderate-intensity cycling compared developed by Gilliam (1995) (ADHD-T) using traditional with following a seated rest condition. While increases in characters (Cheng, 2008) was completed by the parents to assess P3 amplitude may account for improved inhibitory control the severity of ADHD symptoms in each child. Inter-rater following acute bouts of moderate-intensity aerobic exercise in reliability and test-retest reliability of ADHD-T was above 0.9 children with ADHD, to date we have limited understanding and 0.8–0.92, respectively (Cheng, 2008). Those with ADHD of the effects of low- and vigorous-intensity exercises on P3 typically score in the range of 46–155 in this test. Participants amplitudes, or of the differential effects across low, moderate, in the present study had a mean score of 105.72 ± 12.73, and vigorous aerobic exercises on P3 amplitude. Given that indicating a moderate severity of ADHD symptoms (Gilliam, modulations in P3 amplitude are closely related to cortical 1995). In addition, the parent-rated Child Behavior Checklist arousal changes (Kamijo et al., 2004b), it could be speculated (CBCL), which has been used as diagnostic tools to identify that different exercise intensities would differentially modulate clinical disorders and quantify the severity of psychopathology in P3 amplitude. children and adolescents (Chang et al., 2016). The present study The purpose of this current study was to investigate whether adapted the attention problem scale, a subscale of the CBCL, to the effects of acute exercise on inhibitory control would be index ADHD symptom levels. The children in the present study moderated by different exercise intensities. With regards to had t-score of 72.75 ± 9 where a t-value of 60 is considered as the cortical arousal fluctuation, it was hypothesized that arousal cut-off score for the clinical range (Aebi et al., 2010). would increase with exercise intensity, as reflected by decreased Of those recruited, seven participants were excluded from alpha power. Moderate-intensity exercise would result in an the present study. Four of them failed to complete the whole optimal state of cortical arousal, whereas low-and vigorous- experiment and three had <50% accuracy in the task due to (a) intensity exercises would result in a suboptimal state of cortical they did not understand the instructions, (b) felt bored during arousal. Similarly, it was hypothesized that moderate-intensity the task, or (c) displayed disruptive behavior. The criterion of exercise would result in better inhibitory control performance, 50% response accuracy was utilized by a previous study that which could be reflected by shorter RT and/or higher response also focused on children with ADHD (Yu et al., 2020). Of the accuracy, as well as larger P3 amplitude relative to low- remaining 25 children (mean age = 10.54, SD = 1.17), 16 were and vigorous-intensities. taking stimulant medications such as Ritalin (n = 6), Concerta Deficits in inhibitory control and its neuroelectric outcomes (n = 9), and Strattera (n = 1), and they were instructed to are core neurocognitive deficits in children with ADHD abstain from medications for at least 24 h prior to each visit (McAuley et al., 2014) and have negative impacts on various (Johnstone et al., 2009). Of the 25 children, one child was cognitive domains (Miyake et al., 2000). As such, an examination also diagnosed with autism spectrum disorder and the other to whether there is a dose-response relation between acute 24 children did not have any co-morbidities. Before starting aerobic exercise intensity and inhibitory control, as well as experimental sessions, written informed consent and assent an understanding of possible underlying mechanisms that may forms approved by the Institutional Review Board at National drive acute exercise effects, affords a better understanding of the Taiwan University were completed by the parents and children, optimal acute exercise protocols to aid inhibitory control. respectively. The demographic characteristics of participants are summarized in Table 1. MATERIALS AND METHODS Flanker Task Participants The computerized Eriksen flanker task (Eriksen and Eriksen, Thirty-two children from local elementary schools were screened 1974) used in this study incorporated two types of stimulus: following referrals from special education teachers and parents. “congruent,” where all arrows point in the same direction (< This sample size was determined based on an a priori power <<<< or >>>>>) and “incongruent,” where the analysis using G∗Power 3.1 (Faul et al., 2007). Assuming an central target arrow points in a different direction to the adjacent 2 = effect size (ηp 0.33) reported in previous studies (Pontifex arrows (<<><< or >><>>). In addition, cognitive et al., 2013; Ludyga et al., 2017), a sample size of 24 participants loads were varied by instructing participants to complete the was satisfactory to reach a power of 0.80 at an alpha level of task under two different trial conditions, “compatible” and 0.05. Although the power analysis indicated that a sample of “incompatible.” In the “compatible” condition, target arrows 24 children was satisfactory, we recruited 32 participants to pointing left or right required a response using the fingers of compensate for any dropouts, incompliance, or bad data. The the corresponding left or right side. Thus, in a “compatible” inclusion criteria were as follows: (1) the child has had been trail, if the target arrow was facing left, participants were
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TABLE 1 | Demographic characteristics of participants. Upon arrival, parents were instructed to complete the paperwork (an informed consent form, the medication status of the child, Characteristics ADHD (N = 25) and psychological conditions), and the child was instructed to Gender (male/female) 23/2 administer with a battery of physical fitness and motor skill tests Age (yr) 10.54 (1.17) (refer to related test Hsieh et al., 2017), which was not reported in Height (cm) 146.60 (10.25) the current study. Weight (kg) 42.40 (11.53) From Day 2 to 4, participants underwent the low, moderate, BMI 19.37 (2.78) and vigorous exercise sessions in a counterbalanced order. Given Subtype of ADHD N (%) that a growing body of evidence has indicated a positive effect of moderate-intensity exercise on inhibitory control in children, Inattentive 11 (44) including children with ADHD (Suarez-Manzano et al., 2018), Impulsive/hyper 0 (0) we did not include a non-exercise control session in the current Combined 14 (56) study. This decision was made in order to avoid practice or Taking medication 16 (64) familiarization effect, as well as to keep children away from All data presented as mean (SD) unless otherwise noted. becoming bored with the study protocol. In each session, before engaging in exercise (Pre-EX), participants were first seated comfortably on a chair and fitted instructed to press the A button (located on the left side of with an electrode cap and a resting EEG was recorded for 2 min the keyboard) with their left index finger. If the target faced with open (O) eyes of the participant (O) and fixated upon a right, participants were instructed to press the L key (on the cross on the computer screen. Another 2 min of recording was right side of the keyboard) with their right index finger. An then conducted with closed (C) eyes of the participants. This “incompatible” trial required participants to press the A key when was then repeated (i.e., the order of recording was OCOC) one the target arrow faced right and the L key when it faced left. time. A resting HR measure was also taken during this time Cognitive loads were increased in the incompatible condition for later calculation of target HR. This was followed by a 30- since participants were not only required to exhibit inhibitory min exercise session consisting of 5 min of warm-up, 20 min of control, but also cognitive flexibility and working memory exercise, and then a 5-min cool-down period. The same protocol (Chaddock et al., 2012). Varying congruency and compatibility (i.e., exercise with a cap on) has been utilized by several previous produced four experimental conditions: Compatible-Congruent studies (Kamijo et al., 2004b; Pontifex et al., 2015; Hung et al., (CC), Compatible-Incongruent (CI), Incompatible-Congruent 2016; Ludyga et al., 2017; Kao et al., 2018; McGowan et al., 2019; (IC), and Incompatible-Incongruent (II), with CC and CI trials Yu et al., 2020). preceding IC and II trials. The “compatible” and “incompatible” The intervention consisted of low, moderate, or vigorous tasks each consisted of three blocks. Each block was made up of exercises defined as running on a treadmill with a target HR 60 trials with an equal number of congruent and incongruent of 30, 50–60, and 70–80% of individual HR reserve (HRR), stimuli. Each trial began with a central fixation cross (+) lasting respectively. These three exercise intensities were adapted from 1,000 ms, followed by the target stimulus for 200 ms displayed at the classification developed by Norton et al. (2010), where 20– the center of the computer screen. The next trial began after a 40% HRR, 40–60% HRR, and 60–85% HRR represented light, button-press response was made or at the end of the response moderate, and vigorous-intensity exercises, respectively, and are window of 1,200 ms from the time of the presentation of a target aligned with previous studies that also investigated the effects of stimulus. Participants performed all blocks in a single session aerobic exercise on inhibitory control in children with ADHD with a 1 min break between each block. The total duration of the (Chang et al., 2012; Chuang et al., 2015; Yu et al., 2020). HRR flanker task was ∼30 min. was calculated as maximal HR minus resting HR (Karvonen et al., 1957), where the maximal HR was estimated using the Exercise Manipulation Check formula “206.9 – (0.67 × age)” (Gellish, 2007). The target HR was Heart rate was recorded with a Polar HR monitor before the calculated as follows: Target HR = {[(maximal HR– resting HR) exercise session (pre-HR), and then every 30s during the main × percentage intensity desired] + resting HR}. stage (20 min) of 30 min session of exercise (exercise HR). After Following the completion of the interventions, another exercise, HR (post-HR) was recorded during a resting period resting EEG with eyes open was recorded for 2 min (After- prior to performing the flanker task. During the main exercise EX). Participants were then provided with an explanation of the stage, ratings of perceived exertion (RPE) were also taken every flanker task and allowed 10 practice trials. The compatible flanker 2min to estimate perceptions of individuals of the physical task was performed within about 12 min after exercise, and there demands of the exercise (Borg, 1982). was no significant difference in this time interval between the = = 2 = various treatment conditions [F(2, 48) 1.78, p 0.18, and ηp Procedures 0.07] (average time interval: low intensity M = 13.04 ± 4.90 min; Each participant was asked to visit the laboratory at the same moderate intensity M = 11.33 ± 1.94 min; and vigorous intensity time of day on four separate occasions, with at least 3 days apart M = 12.94 ± 4.20 min). This was followed by the incompatible between each visit. On Day 1, parents and their children were task conditions (IC and II), which occurred around 30 min after given a brief introduction to the study by a trained experimenter. exercise, and there was also no significant time difference between
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= = 2 = ± ± ± ± treatment conditions [F(2, 48) 1.63, p 0.21, and ηp 0.06] (71.24 9.61/65.88 8.47; 66.72 10.67/66.88.5 11.58) (average interval time: low intensity M = 31.92 ± 6.33 min; does not differ from each other (ps > 0.05). This suggested that moderate intensity M = 31.03 ± 4.46 min; and vigorous intensity data quality across three exercise conditions could be consistent M = 29.76 ± 4.52 min). Before the incompatible condition of the and homogenous. flanker task, resting EEG was recorded again for 2 min with eyes open and for 2 min with eyes closed (In-task). Note, the present Data Reduction study analyzed only the data recorded with eyes open to compare Behavioral Performance it with the resting EEG after the acute exercise which was The median absolute deviation method suggested by Leys et al. only recorded with eyes open. Upon completion of all sessions, (2013) was used to detect outliers in behavioral performance (RT parents of the participants received US$65 remuneration for their and accuracy) with the deviation threshold set to 2.5, which is participation in the experiment as well as a brief individual report considered moderately conservative (Miller, 1991). Behavioral on the performance of their child. performance was measured in terms of RT for correct responses as well as accuracy (Acc) (the percentage of trials that successfully Electroencephalography Recording responded to target stimulus) of congruent and incongruent Electroencephalographic activity was measured at 30 sites conditions for compatible and incompatible tasks. using a NeuroScan Quik-Cap (Neuro, Inc., Charlotte, NC, USA) according to a modified 10–20 system (Jasper, 1958). Event-Related Potentials and Resting EEG Ongoing EEG activity was referenced to the average of the The EEG/ERP data were processed offline with Scan 4.5 software mastoid (A1, A2), with AFz serving as the ground electrode. (Compumedics USA, Ltd., El Paso, TX, USA). EOG activity Electrooculographic (EOG) activity, potential responses was corrected using the algorithm developed by Semlitsch generated by eye movements, was measured using electrodes et al. (1986) on both ERP and resting EEG data. For ERP placed at the outer canthus of each eye and above and below the recording, epochs were defined as 100 ms prior to the stimulus left orbit. Electrode impedances were kept below 10 k . EEG to 1,500 ms after the stimulus. The baseline was defined as the signals were recorded and sampled at 500 Hz using a DC−100 Hz mean amplitude of the 100 ms pre-stimulus interval. The data filter and a 60 Hz notch filter. were filtered using a 30 Hz low-pass cutoff (12 dB/octave), and Considering the possibility of electrode bridges and non- ERP trials with an amplitude outside the range of ± 100 µV brain derived artifacts when participants exercised with the were excluded. Only correct responses were averaged. The mean EEG caps on, we have several procedures to mitigate these number of trials for each condition was 72.68 ± 8.53 (CC), 67.63 issues. First, before data collection, we adjusted the cap position ± 8.14 (IC), 68.83 ± 9.43 (IC), and 68.75 ± 10.56 (II). Peak if there was any shifting caused by movements. Given that detection was only performed at the Pz electrode from the grand- sweat may continue after exercising, the room temperature averaged waveforms (Figure 1), and this electrode selection was was controlled under 26◦C to avoid excess perspiration. We made by referring to the scalp distribution of P3 (Figure 2) as also do not overfill the gel into each electrode during cap well as previous works (Polich, 2007). P3 latency was defined as preparation to avoid potential bridging between electrodes, the latency of the positive peak between the 300–800ms time especially after exercise with sweat. In addition, the impedance window after stimulus onset. P3 amplitude was defined as the was kept below 10 k for all electrodes. Research indicated mean amplitude within a 50 ms interval surrounding the positive that valid EEG signals could be recorded with impedance <40 peak (Pontifex et al., 2013). k (Ferree et al., 2001) and the conductance of sweat could For resting alpha oscillations, epochs were defined as 2,000 ms. be minimized with an impedance closed to 5 k (Picton and The baseline was defined as the mean amplitude of the entire Hillyard, 1972). Second, during the data processing, we did interval. The data were filtered using a 1–30 Hz band-pass cutoff filtering (filtering out non-brain derived signals or artifacts), (12 dB/octave), and EEG trials with an amplitude outside the baseline correction (could mitigate data drifting caused by sweat), range of ±100 µV were excluded. The mean number of trials and artifact rejection (discarded epochs that contain excess for the time point of vigorous-intensity exercise was 55.82 ± amplitude caused by artifacts), all these protocols could address 9.85 (Pre-EX), 58.32 ± 7.78 (After-EX), and 59.64 ± 5.91 (In- artifacts. Lastly, before averaging the data, we had a visual Task). For the time point of the moderate-intensity exercise, the inspection of all available epochs to see if there were epochs mean number of trials was 56.75 ± 10.78 (Pre-EX), 57.04 ± with bad data. Epochs with bad data would be discarded. We 14.04 (After-EX), and 56.43 ± 13.74 (In-Task). The mean number compared the number of trials included for averaged data across of trials for time point of low-intensity exercise was 57.50 ± three exercise intensity conditions to see whether the trials 9.23 (Pre-EX), 58.43 ± 10.58 (After-EX), and 60.36 ± 6.89 (In- included for finalized data differ as a function of intensity. In Task). The cleaned EEG data were Fast Fourier Transformed and general, greater artifacts would result in a greater number of subsequently log-transformed. The power value for alpha (8– trials being rejected during reduction and artifact rejection. The 13 Hz) at Fz, Cz, and Pz were calculated using fixed frequency mean numbers of accepted congruent/incongruent trials for the bands (Kamijo et al., 2004a). compatible task and incompatible tasks following low-intensity condition (71.60 ± 8.21/68.52 ± 7.08; 69.68 ± 9.72/69.32 ± Statistical Analysis 10.24), moderate-intensity condition (75.20 ± 7.40/68.48 ± 8.81; A repeated-measure ANOVA was utilized to assess the effect 70.08 ± 7.66/70.04 ± 8.92), and vigorous-intensity condition of exercise intensity (i.e., low, moderate, and vigorous exercise)
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FIGURE 1 | Grand-averaged waveforms in CI, CC, IC, and II, respectively. CC, compatible congruent; CI, compatible incongruent; IC, incompatible congruent; II, incompatible incongruent.
FIGURE 2 | Topographic distribution of P3 (400–550 ms). The topographic distribution of P3 amplitude (spectrum: blue to red) is illustrated in CI, CC, IC, and II, respectively. CC, compatible congruent; CI, compatible incongruent; IC, incompatible congruent; II, incompatible incongruent.
Frontiers in Human Neuroscience | www.frontiersin.org 6 June 2021 | Volume 15 | Article 617596 Tsai et al. Exercise Intensity and Inhibitory Control on RPE. The HR changes were further examined by a 3 Behavioral Performance (Time: pre-HR, exercise-HR, and post-HR) × 3 (Intensity: low For RT, there was a significant Intensity × Compatibility = = 2 = exercise, moderate exercise, and vigorous exercise) repeated- interaction [F(2, 48) 4.28, p 0.019, and ηp 0.15]. Follow- measure ANOVA (RM ANOVA). Additionally, a 3 (Intensity) × up analyses indicated longer RT in the incompatible condition 3 (Time: Pre-EX, After-EX, In-task) × 3 (Electrode: Fz, Cz, Pz) regardless of congruency after a session of vigorous-intensity RM ANOVAs were used to test fluctuations in alpha power. To exercise compared to moderate exercise and low exercise test the effects of exercise intensity on behavioral performance sessions, with no difference between the latter two (see Table 3). (i.e., RT and response accuracy), separate 3 (Intensity) × 2 For response accuracy, analysis revealed a significant (Compatibility: compatible and incompatible) × 2(Congruency: Compatibility × Congruency interaction [F(2, 48) = 52.62, p 2 = congruent and incongruent) RM ANOVAs were performed. < 0.001, and ηp 0.69). Follow-up analyses indicated higher Individual (Intensity) × 2(Compatibility) × 2(Congruency) RM response accuracy in CC trials (M = 95.3 %, SD = 3.3%) ANOVAs were conducted to test the effects of exercise intensity compared with CI trials (M = 89.6 %, SD = 4.8%) as well as on P3 amplitude and latency. The Greenhouse-Geisser correction compared with IC trials (M = 91.2%, SD = 2.9%). was used whenever the sphericity assumption was violated. Fisher’s Protected Least Significant Difference (LSD) tests for Neuroelectric Measures multiple comparisons were performed to follow up significant Table 4 summarizes the data relating to P3 latency and effects, an approach considered appropriate when the level of a amplitude. In terms of P3 latency, the analysis found significant factor is < 3 (Baguley, 2012). A family-wise alpha of 0.05 was Intensity × Compatibility × Congruency interactions [F(2, 48) utilized, and effect sizes of ANOVAs were calculated using partial = 4.80, p = 0.013, and η2 = 0.17]. Further decomposition η2 p eta-squared ( p) statistics, and effect sizes for post-hoc of t-tests found a significant Intensity × Congruency interaction in were reported by Cohen’s dz (for within-subject designs). the incompatible condition [F(2, 48) = 4.73, p = 0.016, and To further investigate whether changes in ERP and alpha 2 = ηp 0.17), with longer P3 latencies during the II trials power measures related to changes in behavioral outcomes, compared with IC trials following vigorous (p = 0.04) and Pearson product-moment correlations were performed wherever low intensity exercises (p = 0.02) but not following moderate- significant exercise effects were detected. Data of alpha power intensity exercise. In addition, decomposition found a significant were obtained by subtracting Pre-EX from After-EX as well as Compatibility × Congruency interaction following moderate- subtracting Pre-EX from In-Task to see if the change of alpha = = 2 = intensity exercise [F(1, 24) 7.12, p 0.013, and ηp power is associated with cognitive performance. 0.23], with CC trials having shorter latency compared with CI trials and IC trials. No congruency difference was found RESULTS in the incompatible condition and no compatibility difference was found in the incongruent condition. No Compatibility × Manipulation Check for Exercise Intensity Congruency interaction was observed following vigorous-and Descriptive data for RPE, HR, and alpha values are summarized low-intensity exercises. in Table 2. As expected, there was a significant increase in RPE Regarding P3 amplitude, a significant Compatibility × = 2 = with exercise intensity [F(2, 48) 48.76, p < 0.001, and ηp Congruency interactions [F = 6.07, p = 0.021 and η2 × (1, 24) p 0.67]. An analysis of HR revealed a significant Intensity Time = 0.11] was found. Follow-up analyses indicated larger P3 = 2 = interaction [F(4, 96) 138.29, p < 0.001, and ηp 0.85]. Follow- amplitudes in CI trials compared to CC trials, and II trials up simple main effect analyses found that while exercise-HR compared with IC trials (p’s < 0.04). In addition, there were and post-HR increased with exercise intensity, there were no larger P3 amplitudes in CI trials compared with II trials (p < differences between intensity in pre-HR. 0.001). No intensity associated main effect or interaction effects was observed.
TABLE 2 | Descriptive data for exercise manipulation check and arousal level.
TABLE 3 | Task performance by exercise intensity during compatible and Variable Low Moderate Vigorous P Direction incompatible tasks. M (SD) M (SD) M (SD) Variable Low Moderate Vigorous P Direction RPE 10.32(1.94) 13.03(2.44) 15.06(2.38) <0.001 L
*Data was collapsed across electrode sites. RT, reaction time; Acc, accuracy.
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TABLE 4 | Mean (SD) of event-related brain potential (ERP) data.
Variable P3L P3A Exercise intensity Exercise intensity
Low Moderate Vigorous Low Moderate Vigorous M (SD) M (SD) M (SD) p M (SD) M (SD) M (SD) p
Compatible Congruent 468.72(68.58) 448.32(68.23) 452.16(57.19) n.s. 6.37(2.78) 6.22(2.64) 6.29(3.49) n.s. Incongruent 474.40(63.03) 478.96(59.99) 476.40(59.25) n.s. 7.71(2.85) 7.85(3.25) 7.42(3.93) n.s. Incompatible Congruent 460.72(73.76) 486.56(70.45) 466.75(62.68) n.s. 5.42(3.21) 5.60(3.31) 5.73(2.47) n.s. Incongruent 518.56(74.88) 477.68(76.59) 482.83(55.21) n.s. 6.43(3.62) 6.23(3.89) 5.96(2.81) n.s.
A, amplitude; L, latency.
Arousal Level to examine the role of arousal as a potential mechanism for An analysis of alpha power found a significant interaction effects of exercise intensity on inhibitory control. The results × = 2 = of Intensity Time [F(4, 96) 6.40, p < 0.001, and ηp indicated no difference across exercise intensities in behavioral 0.21). Decomposition of Intensity × Time interaction compared outcomes during the compatible condition. On the other hand, intensity within each time and found significant effects after results also showed longer RT in the incompatible condition exercise (After-EX) and during the flanker task (In-Task). Follow- after a 20 min bout of vigorous-intensity exercise, compared up analyses found mean alpha power decreased with exercise with both low and moderate-intensity exercises. Regarding P3, intensity for both After-EX and In-Task, indicating that there was there is an interference effect following low- and vigorous- a linear increase of cortical arousal with the increase of exercise intensity exercises, which was not seen in the incompatible task intensity 10min or around 30min after exercise (see Table 2). after moderate-intensity exercise. Additionally, cortical arousal Comparing different times within each intensity, the mean alpha increased with greater exercise intensity, as reflected by decreased power decreased during In-Task relative to Pre-EX following alpha power. Similarly, higher cortical arousal was sustained vigorous-intensity exercise, indicating that the arousal level was following vigorous-intensity exercise. In contrast, cortical arousal sustained higher for a while after exercise cessation. However, was decreased following low- and moderate-intensity exercises, the opposite trend was found following low-intensity exercise though in the latter condition the relationship fell short of where the mean alpha power increased in After-EX relative to statistical significance. Lastly, a negative correlation was found Pre-EX (Cohen’s dz = 0.98) as well as In-Task (Cohen’s dz = between changes in arousal level from Pre-Ex to After-Ex and 0,54), indicating that the arousal level was at its lowest level incompatible RT following moderate-intensity exercise. Since we around 10 min after exercise cessation. A similar trend was also did not include a control condition, caution must be exercised found After-EX relative to Pre-EX (Cohen’s dz = 0.48) following in interpreting our findings. However, despite these limitations, moderate-intensity exercise, although this was not statistically the present study does provide preliminary evidence for a dose- significant (p = 0.06) (Figure 3). related effect of aerobic exercise intensity on behavioral and neuroelectric outcomes of inhibitory control in children with Bivariate Correlations ADHD. Our findings are among the first to demonstrate the Given the significant exercise intensity effects were detected moderating role of aerobic exercise intensity on the association of on incompatible RT across congruency trials and alpha power acute aerobic exercise with inhibitory control and cortical arousal change, bivariate correlations were separately calculated between in children with ADHD. incompatible RT and alpha power change under each exercise Results indicated shorter RT in the incompatible condition intensity condition. Results revealed a negative correlation of following low- and moderate-intensity exercises relative to alpha power change from baseline to After-EX with incompatible vigorous-intensity exercise, with no difference between the RT (r = −0.41 and p = 0.45) following the moderate-intensity former two. A lack of difference between low- and moderate- exercise. No other significant correlation between alpha power intensity exercises was unexpected and inconsistent with the change and incompatible RT was found under low-intensity inverted-U hypothesis which predicts that low-intensity exercise condition (r’s = −0.051–0.18 and p’s > 0.80) or vigorous- would result in poorer cognitive performance relative to intensity condition (r’s = 0.005–0.040 and p’s > 0.86). moderate-intensity exercise due to a suboptimal level of cortical arousal. A parallel finding was reported in a pharmaceutical DISCUSSION study, which found that both low and moderate doses of methylphenidate (MPH) had identical positive effects on The purpose of this study was to investigate whether the academic performance (Evans et al., 2001). The study findings effects of acute aerobic exercise on inhibitory control in specific to light-intensity exercise have practical implications children with ADHD are moderated by exercise intensity and since children with ADHD have been found to have a higher risk
Frontiers in Human Neuroscience | www.frontiersin.org 8 June 2021 | Volume 15 | Article 617596 Tsai et al. Exercise Intensity and Inhibitory Control
FIGURE 3 | Topographic distribution of alpha power. The topographic distribution of alpha power (spectrum: blue to red) is illustrated for three intensity exercises and time, respectively. L, low-intensity exercise; M, moderate-intensity exercise; V, vigorous-intensity exercise. of obesity (Cortese et al., 2013). Research has recommended that neural signaling and increases neural noise despite arousal being children with overweight or obesity may have greater adherence high. This dose-related relation between dopamine and cognitive and compliance to light-intensity exercise such as brisk walking, performance is further supported by neuro-pharmacological as compared with more vigorous exercise. Further, a study also findings. For example, MPH and atomoxetine (ATM), two suggests that with higher adherence and better compliance, light common dopaminergic stimulants for children with ADHD, in exercise may manifest equally beneficial effects compared with general, have negative impacts on cognitive performance with exercise with higher intensities in the longer term (Bar-Or, 2000). excessive doses (Gamo et al., 2010; Arnsten and Pliszka, 2011). As such, low-intensity aerobic exercise could be an alternate These findings were inconsistent with previous studies that physical activity choice for children with ADHD, especially showed beneficial effects of vigorous-intensity exercise on children that are less active and are affected by overweight or cognitive performance in children with ADHD (Silva et al., obesity (Tse et al., 2015). 2015; Gawrilow et al., 2016). However, it should be noted that The finding that vigorous-intensity exercise resulted in poorer previous studies did not provide any information on HR or RPE cognitive performance relative to moderate-intensity exercise is to confirm the manipulation of intensity. Therefore, it is not only in line with most previous studies in typically developing children difficult to assess whether the participants did, indeed, participate (Duncan and Johnson, 2014) and adults (Kamijo et al., 2004a,b; in the vigorous-intensity exercise as the authors claimed in Budde et al., 2010; Chang et al., 2011). The poorer cognitive their study, but also make comparisons between these studies performance following vigorous exercise may be explained by and this study impossible. Furthermore, participants in previous neurobiological mechanisms. Exercise results in the secretion of studies engaged in only 5 min of vigorous-intensity exercise, norepinephrine (NE) and dopamine (DA) (Kitaoka et al., 2010; compared with the current study involving 20 min of exercise. It Goekint et al., 2012; see McMorris and Hale, 2015, for review), seems that such a long duration as 20 min of vigorous exercise which stimulates neural signaling (Deutch and Roth, 1990) and might result in fatigue which impaired subsequent inhibitory dampens neural noise (Finlay et al., 1995), respectively, thereby control performance, which was in line with a study in healthy increases vigilance and arousal. However, excessive secretion of young adults (Kamijo et al., 2004a). Notably, the interpretation NE and DA, such as that induced by vigorous exercise, impairs of vigorous-intensity needs to be cautious because we cannot
Frontiers in Human Neuroscience | www.frontiersin.org 9 June 2021 | Volume 15 | Article 617596 Tsai et al. Exercise Intensity and Inhibitory Control indicate the directionality (e.g., impaired following vigorous exercise further enhances inhibitory control via improved neuro- exercise or improved following low and moderate exercise) of inhibition to task-irrelevant information in children with ADHD. exercise effects without a control condition. Consistent with previous studies (Hillman et al., 2009; On the other hand, we did not observe differences across Moore et al., 2013), longer P3 latency and larger P3 amplitude interventions in behavioral measures during the compatible task were observed for the incongruent compared with congruent condition. This finding may imply that, for task components condition, indicating an effective task manipulation so that requiring lower cognitive loads, exercise intensity does not an examination of modulations in P3-ERP after the different moderate task performance in children with ADHD. This intensities of the acute exercise was possible. It is noteworthy that finding supports one previous study that reported improved a congruency effect on P3 latency was observed following low- inhibitory control performance following 20 min bouts of aerobic and vigorous-intensity exercises but not following moderate- exercise regardless of intensity in adults with multiple sclerosis intensity exercise. Since larger congruency effect has been (Sandroff et al., 2016). In summary, our findings suggest that, considered an indication of inefficient interference control in children with ADHD, these three exercise intensities may (Mullane et al., 2009), the findings may indicate that moderate- have similar effects on tasks involving lower cognitive loads, intensity exercise, but not light- or vigorous-intensity exercise, whereas vigorous-intensity aerobic exercise seems to adversely increases interference control and reduces conflicts between task- affect performance on tasks involving high cognitive demand. relevant and irrelevant information at a neurocognitive level. Furthermore, we did not observe any effect of exercise Several limitations of the current study should be intensities on response accuracy during either compatible or acknowledged. First, given the lack of a pre-test assessment incompatible tasks. One review suggests that the effect of or non-exercise control condition, our data could not verify acute exercise on accuracy-dependent measures may depend on whether low and moderate aerobic exercise improves inhibitory the cognitive loads of a cognitive task (McMorris and Hale, control. However, the positive influence of acute aerobic exercise 2012). For example, the Flanker task may be less cognitively on inhibitory control in children with ADHD has been well- demanding as compared with tasks assessing more complex documented by several studies employing a non-exercise control cognitive operations (e.g., planning, abstract, and reasoning), session (Chang et al., 2012; Pontifex et al., 2013; Benzing et al., and, as such, it would be easier for participants to reach a ceiling 2018), and it is reasonable to assume that the beneficial effect effect in their performance (Etnier and Chang, 2009). Future of acute exercise on inhibitory control reported in those studies studies are encouraged to employ cognitive tasks with different would generalize to the present study given the similar exercise levels of complexity to verify whether the effects of exercise on protocols used. Second, the classification of vigorous-intensity response accuracy are dependent on the complexity and nature exercise (i.e., 70–80% of HRR) somewhat overlaps with the of cognitive tasks. moderate intensity in previous studies (50–70% HRR) (Chang Regarding the relationship between exercise intensity and et al., 2012; Hung et al., 2016). Such overlap would lead to an arousal, this study found that arousal, as measured by changes underestimation of the differential effects between moderate and in alpha power, increased with exercise intensity and that vigorous exercise. Despite this, significant differences between the highest arousal level, as reflected by greater decreases these exercise intensities were still observed in measures of HR, in alpha power, was associated with relatively sub-optimal RPE, and arousal level. Third, we only recruited children with the performance. This finding partially supports the arousal- “inattentive” and “combined” subtypes of ADHD, and thus, the performance hypothesis (Cooper, 1973), suggesting that an current finding may not be generalizable to children with other excessive level of cortical arousal induced by vigorous-intensity subtypes of ADHD, such as the hyperactive/impulsive subtype. aerobic exercise might result in relatively poor behavioral Fourth, almost all the participants were boys, which limit the performance. In contrast, there was a moderate increase in generalizability of findings to girls. Last but not least, we did alpha power after both low and moderate-intensity aerobic not take account the medication use of participants. However, exercises. Our data further indicated a negative correlation since all participants were asked to refrain from medication for between changes in alpha power and RT in incompatible flanker at least 24 h before each visit, any confounding effect from the tasks after moderate-intensity exercise, with greater increases in medication was likely to have been minimized. alpha power corresponds to shorter incompatible RT. The results of moderate-intensity aerobic exercise on alpha oscillation align with previous studies that also found increased alpha power CONCLUSION after moderate-intensity exercise (Crabbe and Dishman, 2004; Brummer et al., 2011). Further, the negative association between The present study investigated the acute effects of different alpha power and RT when engaged in incompatible flanker tasks exercise intensities on inhibitory control in children with ADHD may imply that a moderate level of cortical arousal is associated using behavioral indices and P3-ERP. The current findings with better performance on task components requiring greater suggest that children with ADHD may have better inhibitory inhibitory control after moderate-intensity exercise. Increased control following low- and moderate-intensity aerobic exercises alpha power has been found to underpin top-down neuro- relative to vigorous-intensity exercise, and that this may be due to inhibition of task-irrelevant information (Janssens et al., 2018). the suppression of distractors by increased alpha power following As such, while both low- and moderate-intensity aerobic exercise exercise. It should, however, be noted that findings from this may result in optimal cortical arousal, moderate-intensity aerobic study must be interpreted with caution due to the lack of a
Frontiers in Human Neuroscience | www.frontiersin.org 10 June 2021 | Volume 15 | Article 617596 Tsai et al. Exercise Intensity and Inhibitory Control control condition. The 2018U.S. Physical Activity Guidelines University. Written informed consent to participate in this study recommend that acute exercise could serve as an effective means was provided by the participants’ legal guardian/next of kin. in facilitating brain health (U.S. Department of Health Human Services, 2008; Chang et al., 2019). As such, results from this AUTHOR CONTRIBUTIONS study provide further support for the relevance of acute exercise in children with ADHD and provide preliminary evidence for YJT conducted the experiment, analyzed data, and wrote the addressing the optimal level of acute exercise intensity to aid manuscript. SSH interpreted data and revised the manuscript. inhibitory control. CJH and TMH revised critically for important intellectual content. All authors contributed to the article and approved the DATA AVAILABILITY STATEMENT submitted version. The raw data supporting the conclusions of this article will be FUNDING made available by the authors, without undue reservation. This work was particularly supported by the Institute for ETHICS STATEMENT Research Excellence in Learning Sciences of National Taiwan Normal University (NTNU) within the framework of the Higher The studies involving human participants were reviewed and Education Sprout Project by the Ministry of Education (MOE) approved by Institutional Review Board at National Taiwan in Taiwan.
REFERENCES Byun, K., Hyodo, K., Suwabe, K., Ochi, G., Sakairi, Y., Kato, M., et al. (2014). Positive effect of acute mild exercise on executive function via arousal- Aebi, M., Winkler Metzke, C., and Steinhausen, H. C. (2010). Accuracy of related prefrontal activations: an fNIRS study. Neuroimage 98, 336–345. the DSM-oriented attention problem scale of the child behavior checklist doi: 10.1016/j.neuroimage.2014.04.067 in diagnosing attention-deficit hyperactivity disorder. J. Attent. Disord. 13, Chaddock, L., Hillman, C. H., Pontifex, M. B., Johnson, C. R., Raine, L. B., and 454–463. doi: 10.1177/1087054708325739 Kramer, A. F. (2012). Childhood aerobic fitness predicts cognitive performance Arnsten, A. F., and Pliszka, S. R. (2011). Catecholamine influences on prefrontal 1 year later. J. Sports Sci. 30, 421–430. doi: 10.1080/02640414.2011.647706 cortical function: relevance to treatment of attention deficit/hyperactivity Chang, L. Y., Wang, M. Y., and Tsai, P. S. (2016). Diagnostic accuracy of rating disorder and related disorders. Pharmacol. Biochem. Behav. 99, 211–216. scales for attention-deficit/hyperactivity disorder: a meta-analysis. Pediatrics doi: 10.1016/j.pbb.2011.01.020 137:e20152749. doi: 10.1542/peds.2015-2749 Baguley, T. (2012). Serious Stats. Houndmills, Basingstoke, Hampshire; New York, Chang, Y. K., Chu, I. H., Chen, F. T., and Wang, C. C. (2011). Dose-response effect NY: Palgrave Macmillan. doi: 10.1007/978-0-230-36355-7 of acute resistance exercise on Tower of London in middle-aged adults. J. Sport Barkley, R. A. (1997). Behavioral inhibition, sustained attention, and executive Exerc. Psychol. 33, 866–883. doi: 10.1123/jsep.33.6.866 functions: constructing a unifying theory of ADHD. Psychol. Bullet. 121, 65–94. Chang, Y. K., Erickson, K. I., Stamatakis, E., and Hung, T.-M. (2019). How the doi: 10.1037/0033-2909.121.1.65 2018 US physical activity guidelines are a call to promote and better understand Bar-Or, O. (2000). Juvenile obesity, physical activity, and lifestyle changes. Phys. acute physical activity for cognitive function gains. Sports Med. 49, 1625–1627. Sports Med. 28, 51–58. doi: 10.3810/psm.2000.11.1290 doi: 10.1007/s40279-019-01190-x Barry, R. J., Clarke, A. R., and Johnstone, S. J. (2003). A review of Chang, Y. K., and Etnier, J. L. (2009). Exploring the dose-response relationship electrophysiology in attention-deficit/hyperactivity disorder: I. Qualitative between resistance exercise intensity and cognitive function. J. Sport Exerc. and quantitative electroencephalography. Clin. Neurophysiol. 114, 171–183. Psychol. 31, 640–656. doi: 10.1123/jsep.31.5.640 doi: 10.1016/S1388-2457(02)00362-0 Chang, Y. K., Liu, S., Yu, H. H., and Lee, Y. H. (2012). Effect of acute exercise Barry, R. J., Rushby, J. A., Wallace, M. J., Clarke, A. R., Johnstone, S. J., and on executive function in children with attention deficit hyperactivity disorder. Zlojutro, I. (2005). Caffeine effects on resting-state arousal. Clin. Neurophysiol. Archiv. Clin. Neuropsychol. 27, 225–237. doi: 10.1093/arclin/acr094 116, 2693–2700. doi: 10.1016/j.clinph.2005.08.008 Cheng, L. Y. (2008). Attention-Deficit/Hyperactivity Disorder Test: A Method for Benzing, V., Chang, Y. K., and Schmidt, M. (2018). Acute physical activity Identifying Individuals With ADHD. Taipei: Psychological Publishing. enhances executive functions in children with ADHD. Sci. Rep. 8:12382. Chuang, L. Y., Tsai, Y. J., Chang, Y. K., Huang, C. J., and Hung, T. M. (2015). doi: 10.1038/s41598-018-30067-8 Effects of acute aerobic exercise on response preparation in a Go/No Go Biederman, J., Petty, C. R., Clarke, A., Lomedico, A., and Faraone, S. V. (2011). Task in children with ADHD: an ERP study. J. Sport Health Sci. 4, 82–88. Predictors of persistent ADHD: an 11-year follow-up study. J. Psychiatr. Res. doi: 10.1016/j.jshs.2014.11.002 45, 150–155. doi: 10.1016/j.jpsychires.2010.06.009 Cooper, C. J. (1973). Anatomical and physiological mechanisms of arousal, Borg, G. A. V. (1982). Psychophysical bases of perceived exertion. Med. with special reference to the effects of exercise. Ergonomics 16, 601–609. Sci. Sports Exerc. 14, 377–381. doi: 10.1249/00005768-198205000- doi: 10.1080/00140137308924551 00012 Cortese, S., Ramos Olazagasti, M. A., Klein, R. G., Castellanos, F. X., Proal, Brummer, V., Schneider, S., Abel, T., Vogt, T., and Struder, H. K. (2011). Brain E., and Mannuzza, S. (2013). Obesity in men with childhood ADHD: cortical activity is influenced by exercise mode and intensity. Med. Sci. Sports a 33-year controlled, prospective, follow-up study. Pediatrics 2012:540. Exerc. 43, 1863–1872. doi: 10.1249/MSS.0b013e3182172a6f doi: 10.1542/peds.2012-0540 Budde, H., Voelcker-Rehage, C., Pietrassyk-Kendziorra, S., Machado, S., Crabbe, J. B., and Dishman, R. K. (2004). Brain electrocortical activity during Ribeiro, P., and Arafat, A. M. (2010). Steroid hormones in the saliva and after exercise: a quantitative synthesis. Psychophysiology 41, 563–574. of adolescents after different exercise intensities and their influence on doi: 10.1111/j.1469-8986.2004.00176.x working memory in a school setting. Psychoneuroendocrinology 35, 382–391. Davey, C. P. (1973). Physical exertion and mental performance. Ergonomics 16, doi: 10.1016/j.psyneuen.2009.07.015 595–599. doi: 10.1080/00140137308924550
Frontiers in Human Neuroscience | www.frontiersin.org 11 June 2021 | Volume 15 | Article 617596 Tsai et al. Exercise Intensity and Inhibitory Control
Deutch, A. Y., and Roth, R. H. (1990). The determinants of stress-induced AD/HD: a visual ERP investigation. Int. J. Psychophysiol. 72, 145–153. activation of the prefrontal cortical dopamine system. Prog. Brain Res. doi: 10.1016/j.ijpsycho.2008.11.007 85, 367–402. Johnstone, S. J., and Galletta, D. (2013). Event-rate effects in the flanker task: Doehnert, M., Brandeis, D., Imhof, K., Drechsler, R., and Steinhausen, H.-C. ERPs and task performance in children with and without AD/HD. Int. J. (2010). Mapping attention-deficit/hyperactivity disorder from childhood Psychophysiol. 87, 340–348. doi: 10.1016/j.ijpsycho.2012.07.170 to adolescence—no neurophysiologic evidence for a developmental Kamijo, K., Nishihira, Y., Hatta, A., Kaneda, T., Kida, T., Higashiura, T., et al. lag of attention but some for inhibition. Biol. Psychiatry 67, 608–616. (2004a). Changes in arousal level by differential exercise intensity. Clin. doi: 10.1016/j.biopsych.2009.07.038 Neurophysiol. 115, 2693–2698. doi: 10.1016/j.clinph.2004.06.016 Duncan, M., and Johnson, A. (2014). The effect of differing intensities of acute Kamijo, K., Nishihira, Y., Hatta, A., Kaneda, T., Wasaka, T., Kida, T., cycling on preadolescent academic achievement. Eur. J. Sport Sci. 14, 279–286. et al. (2004b). Differential influences of exercise intensity on information doi: 10.1080/17461391.2013.802372 processing in the central nervous system. Eur. J. Appl. Physiol. 92, 305–311. Eriksen, B. A., and Eriksen, C. W. (1974). Effects of noise letters upon the doi: 10.1007/s00421-004-1097-2 identification of a target letter in a nonsearch task. Percept. Psychophys. 16, Kao, S. C., Drollette, E. S., Ritondale, J. P., Khan, N., and Hillman, C. H. (2018). 143–149. doi: 10.3758/BF03203267 The acute effects of high-intensity interval training and moderate-intensity Etnier, J. L., and Chang, Y.-K. (2009). The effect of physical activity on continuous exercise on declarative memory and inhibitory control. Psychol. executive function: a brief commentary on definitions, measurement issues, Sport Exerc. 38, 90–99. doi: 10.1016/j.psychsport.2018.05.011 and the current state of the literature. J. Sport Exerc. Psychol. 31, 469–483. Karvonen, M., Kentala, E., and Mustala, O. (1957). The effects of training on doi: 10.1123/jsep.31.4.469 heart rate; a longitudinal study. Annales medicinae experimentalis et biologiae Evans, S. W., Pelham, W. E., Smith, B. H., Bukstein, O., Gnagy, E. M., Fenniae. 35, 307–315. Greiner, A. R., et al. (2001). Dose–response effects of methylphenidate Kitaoka, R., Fujikawa, T., Miyaki, T., Matsumura, S., Fushiki, T., and Inoue, K. on ecologically valid measures of academic performance and classroom (2010). Increased noradrenergic activity in the ventromedial hypothalamus behavior in adolescents with ADHD. Exp. Clin. Psychopharmacol. 9, 163–175. during treadmill running in rats. J. Nutr. Sci. Vitaminol. 56, 185–190. doi: 10.1037/1064-1297.9.2.163 doi: 10.3177/jnsv.56.185 Faul, F., Erdfelder, E., Lang, A.-G., and Buchner, A. (2007). G∗ Power 3: a flexible Kratz, O., Studer, P., Malcherek, S., Erbe, K., Moll, G. H., and Heinrich, H. (2011). statistical power analysis program for the social, behavioral, and biomedical Attentional processes in children with ADHD: an event-related potential sciences. Behav. Res. Methods 39, 175–191. doi: 10.3758/BF03193146 study using the attention network test. Int. J. Psychophysiol. 81, 82–90. Ferree, T. C., Luu, P., Russell, G. S., and Tucker, D. M. (2001). Scalp electrode doi: 10.1016/j.ijpsycho.2011.05.008 impedance, infection risk, and EEG data quality. Clin. Neurophysiol. 112, Laufs, H., Holt, J. L., Elfont, R., Krams, M., Paul, J. S., Krakow, K., et al. 536–544. doi: 10.1016/S1388-2457(00)00533-2 (2006). Where the BOLD signal goes when alpha EEG leaves. Neuroimage 31, Finlay, J. M., Zigmond, M. J., and Abercrombie, E. D. (1995). Increased 1408–1418. doi: 10.1016/j.neuroimage.2006.02.002 dopamine and norepinephrine release in medial prefrontal cortex induced Leys, C., Ley, C., Klein, O., Bernard, P., and Licata, L. (2013). Detecting outliers: do by acute and chronic stress: effects of diazepam. Neuroscience 64, 619–628. not use standard deviation around the mean, use absolute deviation around the doi: 10.1016/0306-4522(94)00331-X median. J. Exp. Soc. Psychol. 49, 764–766. doi: 10.1016/j.jesp.2013.03.013 Gamo, N. J., Wang, M., and Arnsten, A. F. T. (2010). Methylphenidate Lin, Y. J., and Gau, S. S. (2018). Developmental changes of neuropsychological and atomoxetine enhance prefrontal function through α2-adrenergic and functioning in individuals with and without childhood ADHD from early dopamine D1 receptors. J. Am. Acad. Child Adolesc. Psychiatry 49, 1011–1023. adolescence to young adulthood: a 7-year follow-up study. Psychol. Med. 2018, doi: 10.1016/j.jaac.2010.06.015 1–12. doi: 10.1017/S0033291718001599 Gawrilow, C., Stadler, G., Langguth, N., Naumann, A., and Boeck, A. (2016). Liotti, M., Pliszka, S. R., Higgins, K., Perez, R. R., and Semrud-Clikeman, M. (2010). Physical activity, affect, and cognition in children with symptoms of ADHD. Evidence for specificity of ERP abnormalities during response inhibition in J. Attent. Disord. 20, 151–162. doi: 10.1177/1087054713493318 ADHD children: a comparison with reading disorder children without ADHD. Gellish, R. L., Goslin, B. R., Olson, R. E., McDonald, A., Russi, G. D., Brain Cogn. 72, 228–237. doi: 10.1016/j.bandc.2009.09.007 and Moudgil, V. K. (2007). Longitudinal modeling of the relationship Liu, Y., Hanna, G. L., Hanna, B. S., Rough, H. E., Arnold, P. D., and between age and maximal heart rate. Med. Sci. Sports Exerc. 39, 822–829. Gehring, W. J. (2020). Behavioral and electrophysiological correlates of doi: 10.1097/mss.0b013e31803349c6 performance monitoring and development in children and adolescents Gilliam, J. E. (1995). Attention-Deficit Hyperactivity Disorder Test: A Method for with attention-deficit/hyperactivity disorder. Brain Sci. 10:20079. Identifying Individuals With ADHD: Examiner’s Manual. Austin, TX: Pro-Ed. doi: 10.3390/brainsci10020079 Goekint, M., Bos, I., Heyman, E., Meeusen, R., Michotte, Y., and Sarre, S. (2012). Luck, S. J. (2014). An Introduction to the Event-Related Potential Technique. Acute running stimulates hippocampal dopaminergic neurotransmission in Cambridge, MA: MIT press. rats, but has no influence on brain-derived neurotrophic factor. J. Appl. Physiol. Ludyga, S., Brand, S., Gerber, M., Weber, P., Brotzmann, M., Habibifar, F., et al. 112, 535–541. doi: 10.1152/japplphysiol.00306.2011 (2017). An event-related potential investigation of the acute effects of aerobic Hillman, C. H., Buck, S. M., Themanson, J. R., Pontifex, M. B., and Castelli, and coordinative exercise on inhibitory control in children with ADHD. Dev. D. M. (2009). Aerobic fitness and cognitive development: event-related brain Cogn. Neurosci. 28, 21–28. doi: 10.1016/j.dcn.2017.10.007 potential and task performance indices of executive control in preadolescent Mahon, A. D., Dean, R. S., McIntosh, D. E., Marjerrison, A. D., Cole, A. S., children. Dev. Psychol. 45, 114–129. doi: 10.1037/a0014437 Woodruff, M. E., et al. (2013). Acute exercise effects on measures of attention Hsieh, S. S., Lin, C. C., Chang, Y. K., Huang, C. J., and Hung, T. M. (2017). Effects and impulsivity in children with attention deficit/hyperactivity disorder. J. of childhood gymnastics program on spatial working memory. Med. Sci. Sports Educ. Dev. Psychol. 3:65. doi: 10.5539/jedp.v3n2p65 Exerc. 49, 2537–2547. doi: 10.1249/MSS.0000000000001399 McAuley, T., Crosbie, J., Charach, A., and Schachar, R. (2014). The persistence Hung, C. L., Huang, C.-J., Tsai, Y.-J., Chang, Y.-K., and Hung, T.-M. (2016). of cognitive deficits in remitted and unremitted ADHD: a case for the state- Neuroelectric and behavioral effects of acute exercise on task switching in independence of response inhibition. J. Child Psychol. Psychiatry 55, 292–300. children with attention-deficit/hyperactivity disorder. Front. Psychol. 7:1589. doi: 10.1111/jcpp.12160 doi: 10.3389/fpsyg.2016.01589 McGowan, A. L., Chandler, M. C., Brascamp, J. W., and Pontifex, M. B. Janssens, C., De Loof, E., Boehler, C. N., Pourtois, G., and Verguts, T. (2018). (2019). Pupillometric indices of locus-coeruleus activation are not modulated Occipital alpha power reveals fast attentional inhibition of incongruent following single bouts of exercise. Int. J. Psychophysiol. 140, 41–52. distractors. Psychophysiology 55:e13011. doi: 10.1111/psyp.13011 doi: 10.1016/j.ijpsycho.2019.04.004 Jasper, H. H. (1958). The ten twenty electrode system of the international McMorris, T., and Hale, B. J. (2012). Differential effects of differing intensities federation. Electroencephalogr. Clin. Neurophysiol. 10, 371–375. of acute exercise on speed and accuracy of cognition: a meta-analytical Johnstone, S. J., Barry, R. J., Markovska, V., Dimoska, A., and Clarke, A. investigation. Brain Cogn. 80, 338–351. doi: 10.1016/j.bandc.2012. R. (2009). Response inhibition and interference control in children with 09.001
Frontiers in Human Neuroscience | www.frontiersin.org 12 June 2021 | Volume 15 | Article 617596 Tsai et al. Exercise Intensity and Inhibitory Control
McMorris, T., and Hale, B. J. (2015). Is there an acute exercise-induced Rowe, D. L., Robinson, P. A., Lazzaro, I. L., Powles, R. C., Gordon, E., and physiological/biochemical threshold which triggers increased speed of Williams, L. M. (2005). Biophysical modeling of tonic cortical electrical activity cognitive functioning? A meta-analytic investigation. J. Sport Health Sci. 4, in attention deficit hyperactivity disorder. Int. J. Neurosci. 115, 1273–1305. 4–13. doi: 10.1016/j.jshs.2014.08.003 doi: 10.1080/00207450590934499 Medina, J. A., Netto, T. L., Muszkat, M., Medina, A. C., Botter, D., Orbetelli, Sandroff, B. M., Hillman, C. H., Benedict, R. H., and Motl, R. W. (2016). Acute R., et al. (2010). Exercise impact on sustained attention of ADHD effects of varying intensities of treadmill walking exercise on inhibitory control children, methylphenidate effects. Attent. Deficit Hyperactiv. Disord. 2, 49–58. in persons with multiple sclerosis: a pilot investigation. Physiol. Behav. 154, doi: 10.1007/s12402-009-0018-y 20–27. doi: 10.1016/j.physbeh.2015.11.008 Miller, J. (1991). Reaction time analysis with outlier exclusion: bias Satterfield, J. H., Cantwell, D. P., and Satterfield, B. T. (1974). Pathophysiology varies with sample size. Quart. J. Exp. Psychol. 43, 907–912. of the hyperactive child syndrome. Arch. Gen. Psychiatry 31, 839–844. doi: 10.1080/14640749108400962 doi: 10.1001/archpsyc.1974.01760180079010 Miyake, A., Friedman, N. P., Emerson, M. J., Witzki, A. H., Howerter, A., and Semlitsch, H. V., Anderer, P., Schuster, P., and Presslich, O. (1986). A solution Wager, T. D. (2000). The unity and diversity of executive functions and their for reliable and valid reduction of ocular artifacts, applied to the P300 ERP. contributions to complex “Frontal Lobe” tasks: a latent variable analysis. Cogn. Psychophysiology 23, 695–703. doi: 10.1111/j.1469-8986.1986.tb00696.x Psychol. 41, 49–100. doi: 10.1006/cogp.1999.0734 Silva, A. P., Prado, S. O. S., Scardovelli, T. A., Boschi, S. R. M. S., Campos, L. Moore, R. D., Wu, C. T., Pontifex, M. B., O’Leary, K. C., Scudder, M. R., C., and Frère, A. F. (2015). Measurement of the effect of physical exercise Raine, L. B., et al. (2013). Aerobic fitness and intra-individual variability on the concentration of individuals with ADHD. PLoS ONE 10:122119. of neurocognition in preadolescent children. Brain Cogn. 82, 43–57. doi: 10.1371/journal.pone.0122119 doi: 10.1016/j.bandc.2013.02.006 Strauß, M., Ulke, C., Paucke, M., Huang, J., Mauche, N., Sander, C., et al. (2018). Mullane, J. C., Corkum, P. V., Klein, R. M., and McLaughlin, E. (2009). Brain arousal regulation in adults with attention-deficit/hyperactivity disorder Interference control in children with and without ADHD: a systematic review (ADHD). Psychiatry Res. 261, 102–108. doi: 10.1016/j.psychres.2017.12.043 of Flanker and Simon task performance. Child Neuropsychol. 15, 321–342. Suarez-Manzano, S., Ruiz-Ariza, A., De La Torre-Cruz, M., and Martinez-Lopez, doi: 10.1080/09297040802348028 E. J. (2018). Acute and chronic effect of physical activity on cognition and Northey, J. M., Cherbuin, N., Pumpa, K. L., Smee, D. J., and Rattray, B. behaviour in young people with ADHD: a systematic review of intervention (2018). Exercise interventions for cognitive function in adults older than studies. Res. Dev. Disabil. 77, 12–23. doi: 10.1016/j.ridd.2018.03.015 50: a systematic review with meta-analysis. Br. J. Sports Med. 52, 154–160. Tse, A. C. Y., Wong, T. W. L., and Lee, P. H. (2015). Effect of low-intensity exercise doi: 10.1136/bjsports-2016-096587 on physical and cognitive health in older adults: a systematic review. Sports Norton, K., Norton, L., and Sadgrove, D. (2010). Position statement on physical Med. Open 1:37. doi: 10.1186/s,40798-015-0034-8 activity and exercise intensity terminology. J. Sci. Med. Sport 13, 496–502. U.S. Department of Health and Human Services (2008). Physical Activity doi: 10.1016/j.jsams.2009.09.008 Guidelines for Americans. 2nd edn. Washington, DC: US Department of Health Oberste, M., Javelle, F., Sharma, S., Joisten, N., Walzik, D., Bloch, W., et al. and Human Services. (2019). Effects and moderators of acute aerobic exercise on subsequent Willcutt, E. G., Doyle, A. E., Nigg, J. T., Faraone, S. V., and Pennington, interference control: a systematic review and meta-analysis. Front. Psychol. B. F. (2005). Validity of the executive function theory of attention- 10:2616. doi: 10.3389/fpsyg.2019.02616 deficit/hyperactivity disorder: a meta-analytic review. Biol. Psychiatry 57, Oken, B. S., Salinsky, M. C., and Elsas, S. M. (2006). Vigilance, alertness, or 1336–1346. doi: 10.1016/j.biopsych.2005.02.006 sustained attention: physiological basis and measurement. Clin. Neurophysiol. Yu, C. L., Hsieh, S. S., Chueh, T. Y., Huang, C. J., Hillman, C. H., and Hung, 117, 1885–1901. doi: 10.1016/j.clinph.2006.01.017 T. M. (2020). The effects of acute aerobic exercise on inhibitory control and Picton, T., and Hillyard, S. (1972). Cephalic skin potentials in resting state heart rate variability in children with ADHD. Sci. Rep. 10:19958. electroencephalography. Electroencephalogr. Clin. Neurophysiol. 33, 419–424. doi: 10.1038/s41598-020-76859-9 doi: 10.1016/0013-4694(72)90122-8 Zentall, S. S., and Zentall, T. R. (1983). Optimal stimulation: a model of disordered Piepmeier, A. T., Shih, C.-H., Whedon, M., Williams, L. M., Davis, M. E., activity and performance in normal and deviant children. Psychol. Bullet. Henning, D. A., et al. (2015). The effect of acute exercise on cognitive 94:446. doi: 10.1037/0033-2909.94.3.446 performance in children with and without ADHD. J. Sport Health Sci. 4, Zhang, D. W., Johnstone, S. J., Roodenrys, S., Luo, X., Li, H., Wang, E., 97–104. doi: 10.1016/j.jshs.2014.11.004 et al. (2018). The role of resting-state EEG localized activation and central Polich, J. (2007). Updating P300: an integrative theory of P3a and nervous system arousal in executive function performance in children with P3b. Clin. Neurophysiol. 118, 2128–2148. doi: 10.1016/j.clinph.2007. Attention-Deficit/Hyperactivity Disorder. Clin. Neurophysiol. 129, 1192–1200. 04.019 doi: 10.1016/j.clinph.2018.03.009 Pontifex, M. B., Parks, A. C., Henning, D. A., and Kamijo, K. (2015). Single bouts of exercise selectively sustain attentional processes. Psychophysiology 52, 618–625. Conflict of Interest: The authors declare that the research was conducted in the doi: 10.1111/psyp.12395 absence of any commercial or financial relationships that could be construed as a Pontifex, M. B., Saliba, B. J., Raine, L. B., Picchietti, D. L., and Hillman, potential conflict of interest. C. H. (2013). Exercise improves behavioral, neurocognitive, and scholastic performance in children with attention-deficit/hyperactivity disorder. J. Copyright © 2021 Tsai, Hsieh, Huang and Hung. This is an open-access article Pediatr. 162, 543–551. doi: 10.1016/j.jpeds.2012.08.036 distributed under the terms of the Creative Commons Attribution License (CC BY). Rapport, M., Bolden, J., Kofler, M., Sarver, D., Raiker, J., and Alderson, R. The use, distribution or reproduction in other forums is permitted, provided the M. (2009). Hyperactivity in boys with attention-deficit/hyperactivity disorder original author(s) and the copyright owner(s) are credited and that the original (ADHD): a ubiquitous core symptom or manifestation of working memory publication in this journal is cited, in accordance with accepted academic practice. deficits? J. Abnorm. Child Psychol. 37, 521–534. doi: 10.1007/s10802-008- No use, distribution or reproduction is permitted which does not comply with these 9287-8 terms.
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